Seasonal Fruit Preferences for Lipids and Sugars by American Robins

—Fruit preference by birds is a complex process based upon the morphology and spatial arrangement of fruits and on the physiological needs and capabilities of birds. In North America, most fruits can be divided into two groups based on nutritional content: those rich in sugars relative to lipids, and those rich in lipids relative to sugars. To investigate how fruit preference may change seasonally and to determine if it is correlated with physiological state, we designed a simple laboratory experiment using American Robins (Turdus migratorius) and artificial fruits. During summer and autumn, we offered eight robins a choice between synthetic sugar-rich and lipid-rich fruits of equal caloric value and then measured food intake and assimilation efficiency for each fruit type. Overall, robins preferred sugar-rich to lipid-rich fruits during both seasons. Robins had a higher assimilation efficiency for sugars than for lipids during both seasons, although assimilation efficiency of lipids increased significantly from summer to autumn. During experiments, robins consumed significantly more sugar-rich than lipid-rich fruits in summer but not in autumn. Coupling fruit intake with assimilation efficiency indicates that in summer, robins had a higher rate of energy gain from sugars than from lipids, but by autumn the rate of energy gain from lipids increased to nearly the same level as that from sugars. Our results suggest that robins prefer sugar-rich fruits because of their simple and fast rate of digestion, enabling higher rates of energy gain, but that lipid-rich fruits become important with the onset of autumn. Received 5 February 1999, accepted 14 December 1999. ONE MECHANISM used by plants to disperse their seeds is the reward of fleshy fruit pulp to frugivorous animals (Howe 1986). In turn, this reward provides a primary source of energy for the frugivore. Hence, frugivory has concomitant consequences for plant and animal. Because of these consequences, the question of what determines fruit preference and selection by frugivores has long been a central question of foraging ecology. Most studies of fruit selection by frugivorous birds have approached the question as an optimal foraging problem. Frugivores are expected to choose the most profitable fruits, and 1 Present address: Department of Fisheries and Wildlife, Michigan State University, 13 Natural Resources Building, East Lansing, Michigan 48824, USA. E-mail: [email protected] 2 Present address: Department of Biology, University of Virginia, Charlottesville, Virginia 22903, USA. 3 Present address: Department of Forest Resources, Oregon State University, Corvallis, Oregon 97331, USA. 4 Present address: Department of Entomology, Oregon State University, Corvallis, Oregon 97331, USA. studies have found preferences based on caloric content (Sorensen 1984, Johnson et al. 1985, McPherson 1987), concentration of major nutrients (Denslow 1987, Levey 1987, Jung 1992), pulpto-seed ratio (Howe and Vande Kerckhove 1980, Herrera 1982, Murray et al. 1993), fruit size (Paszkowski 1982), seed-passage rates (Sorensen 1984, Levey and Grajal 1991), fruit color (Turček 1963, Wheelwright and Janson 1985, Willson et al. 1990), secondary chemicals (Sorensen 1983, Cipollini and Levey 1997, Levey and Cipollini 1998), microbial infection (Buchholz and Levey 1990), abundance/crop size (Snow 1971, Howe and Estabrook 1977, Murray 1987, Sallabanks 1992), and accessibility (Denslow and Moermond 1982, Moermond and Denslow 1983). Furthermore, fruit selection is not based solely on characteristics of the fruit itself, but also on the bird’s ability to digest the fruit (Levey and Karasov 1989, Martı́nez del Rio and Karasov 1990). Thus, fruit selection is a complex process that is based on interactions among the morphology and spatial arrangement of fruits and the physiological needs and capabilities of birds. As seasons change, corresponding changes 710 [Auk, Vol. 117 LEPCZYK ET AL. occur in the physiological needs of frugivorous birds (Terrill 1990). One notable change occurs in late summer and early autumn when migratory birds build energy reserves to prepare for departure (Bairlein and Gwinner 1994). However, just as the physiological needs of the birds change seasonally, so do the fruits themselves. Specifically, fruits in North America can be divided into two broad groups based on nutritional content: those that are high in sugar relative to lipids, and those that are high in lipids relative to sugars (Stiles 1980, Herrera 1982). These two classes of fruits have a slight temporal difference in their occurrence, with sugar-rich fruits being common throughout the fruiting season (i.e. summer through early winter) and lipid-rich fruits being common primarily in late summer through early winter (Stiles 1980, Herrera 1982). Notably, the lipidrich fruiting season is most prominent during the time when autumn migration occurs, suggesting a potential mutualistic relationship. Because most migratory birds depend on internally stored fat for fuel, they must accumulate large reserves prior to migration (Bairlein and Gwinner 1994). As such, a dietary preference may exist for lipid-rich fruits in the weeks or days before migration. Moreover, because lipids (ca. 39 kJ/g) contain more energy per unit mass than sugars (ca. 17 kJ/g; Guyton 1986), foraging theory predicts that lipid-rich fruits would be preferred to sugar-rich fruits, all else being equal, during all seasons. However, the efficiency with which lipids and sugars are digested and assimilated may differ. Thus, the question of which nutrients migratory birds select is of key interest in terms of foraging theory and bird physiology. To investigate if fruit preferences change seasonally and are related to digestibility, we designed a simple laboratory experiment using migratory American Robins (Turdus migratorius). Because fruit choice may result from the combined effects of nutritional and non-nutritional factors (Baird 1980, Foster 1990), we eliminated as many extrinsic factors as possible by constructing synthetic fruits of equal caloric value that differed only in the relative amounts of sugars and lipids. We predicted that robins would choose the fruits that were most profitable (i.e. producing the highest rate of energy gain) during each season, and that during autumn the most profitable fruits would be the lipid-rich ones.